physiology of a plant invasion: biomass production, growth ... et al-physiology of a plant...

Physiology of a plant invasion: biomass production, growth and tissuechemistry of invasive and native Phragmites australis populations

Fyziologie rostlinných invazí: produkce biomasy, růst a chemismus pletiv invazních a původních populacíPhragmites australis

Petr Pyšek1,2, Hana Skálová1, Jan Čuda1, Wen-Yong Guo1,3, Jan Doležal1,4, OndřejKauzál1, Carla Lambertini3,5, Klára Pyšková1,2, Hans Brix3 & Laura A. Meyerson6

1The Czech Academy of Sciences, Institute of Botany, CZ-252 43 Průhonice, Czech

Republic; email: [email protected]; 2Department of Ecology, Faculty of Science,

Charles University, Viničná 7, CZ-128 44 Prague, Czech Republic; 3Department of Bio-

science, Faculty of Science, Aarhus University, Ole Worms Alle 1, DK-8000 Aarhus C,

Denmark; 4Museum and Gallery of the Orlické hory Mts, Jiráskova 2, CZ-516 01

Rychnov nad Kněžnou, Czech Republic; 5Department of Agricultural Science, University

of Bologna, Via Fanin 44, 40127 Bologna, Italy; 6The University of Rhode Island,

Department of Natural Resources Science, Kingston, RI, 02881 USA

Pyšek P., Skálová H., Čuda J., Guo W.-Y., Doležal J., Kauzál O., Lambertini C., Pyšková K., BrixH. & Meyerson L. A. (2019) Physiology of a plant invasion: biomass production, growth and tis-sue chemistry of invasive and native Phragmites australis populations. – Preslia 91: 51–75.

Differentiation within Phragmites australis, one of the world’s most cosmopolitan and globallyimportant wild plants, and invasions by individual lineages outside of their native ranges isattracting the interest of scientists worldwide. We compared the physiological performance of 89populations representing distinct genotypes from six phylogeographic groups from Australia,Europe, North America (two groups including native and invasive populations introduced fromEurope), South Africa and Far East in a common garden experiment. We show that the popula-tions cluster into two distinct groups: one that includes populations from Europe and Far Easttogether with the North American invasive, and the second the North American native popula-tions with those from Australia and South Africa. Populations within the former group exhibitedsuperior performance in the following traits: they were more vigorous in terms of higher shootnumber per pot, greater belowground biomass, longer rhizomes, had greater specific leaf area(SLA), higher N and P concentrations in tissues, and greater investment into generative reproduc-tion. Pooled across phylogeographic groups, P. australis has higher values of maximal photosyn-thesis (Amax), higher N and P concentrations in tissues, and greater SLA than most vascular plants,represented by the GLOPNET dataset. Whether due to a weak environmental match or geneticdifferences, the results indicate that invasion by Australian and African populations in the North-ern Hemisphere seems unlikely at present. However, it is not possible to exclude the invasion ofgenotypes of European origin into Southern Hemisphere or other temperate regions.

K e y w o r d s: below- and aboveground biomass, climate, common reed, growth traits, intraspecificdifferentiation, N and P concentrations, photosynthesis, Phragmites australis, phylogeography,physiological traits, plant invasion, specific leaf area

Preslia 91: 51–75, 2019 51

doi: 10.23855/preslia.2019.051

Introduction

Extending from the tropics to cold temperate regions in both hemispheres, Phragmites

australis is among the world’s most cosmopolitan and globally important wild plants(Meyerson et al. 2016b, Eller et al. 2017). Its wide geographic distribution and history ofintroductions make it ideally suited as a model species for studying biogeographicalaspects of plant invasions (van Kleunen et al. 2015, Meyerson et al. 2016b, Pyšek et al.2017). In its native range, it is an important component of wildlife habitats, a keystonespecies with often substantial effects on ecosystem composition and functioning, andprovider of ecosystem services (Packer et al. 2017). However, where introduced, itbecomes a noxious invader diminishing biodiversity and altering ecosystem functionsbut also providing some ecosystem services. This is true namely for North America,where it has rapidly spread over the last two centuries and has converted botanicallydiverse wetlands into low-diversity stands (Meyerson et al. 2000). Introduced Phragmites

is a highly successful invasive grass that has overwhelmed coastal and inland ecosystemsacross much of the United States and southern Canada (see Meyerson et al. 2009 fora review of the situation in North America).

Four distinct lineages of P. australis are present in North America (Meyerson et al.2010, Lambertini et al. 2016): (i) native P. australis subsp. americanus (Saltonstall 2002)is found throughout the United States and much of Canada, where it has been present,inferred from fossil evidence, for at least 40,000 yr (Hansen 1978). Three other lineageshave been identified: (ii) one from Eurasia first appeared in the herbarium record in the19th century and has invaded throughout North America, (iii) the second, P. australis var.berlandieri, is found in the southern United States from Florida to California and alsoextends into Central America and (iv) the third is another recent introduction from theMediterranean region, so far established only in the Mississippi River delta and in a fewmore spots in Florida (Lambertini et al. 2012a). Overall, North America is the most stud-ied region in terms of genetics and much less attention has been paid to other parts of theworld where the species is also widely distributed, in particular Australia, Far East andSouth Africa.

The genetic evidence suggests that there are differences in the biogeographic nichesamong haplotypes (Lambertini et al. 2006, 2012a, Guo et al. 2014, Cronin et al. 2015).This makes P. australis a useful model species for understanding differences between theperformance in native and non-native biogeographic ranges of population groups repre-sented by different genotypes (Kueffer et al. 2013, Meyerson et al. 2016a, Packer et al.2017). However, little is known about how genetic differences among haplotypes trans-late into ecological and physiological differences that determine the vigour of individualpopulations, an attribute that is likely to play a key role in this species’ invasion.

Besides an extensive body of literature on the ecology of P. australis from all over theworld (see Eller et al. 2017, Packer et al. 2017 for recent reviews), and intensive researchinto the mechanisms of its invasion in the United States (e.g. Saltonstall 2002, Guo et al.2013, 2016, 2018, Meyerson et al. 2016b, Pyšek et al. 2018), comparative ecologicalstudies on trait variation under standard conditions have provided valuable knowledgeconcerning the role of phylogeographic diversity in adaptation processes (Hansen et al.2007, Eller et al. 2013, 2014, Nguyen et al. 2013, Guo et al. 2014, Tripathee & Schäfer2014, Allen et al. 2016, Bhattarai et al. 2016, Bui et al. 2016, Mozdzer et al. 2016,

52 Preslia 91: 51–75, 2019

Mozdzer & Caplan 2018, Ren et al. 2018). However, these studies used mainly clonesfrom Europe and North America, and to a limited extent from Australia. We are not awareof any study that would compare these clones with those from other parts of the world.

Here we present data on six P. australis phylogeographic groups, covering the speciestemperate distribution range. Based on a several-year common-garden experiment, weaimed to find the among population-group differences and within population-group vari-ation in traits related to growth, above- and belowground biomass, concentrations ofchemical elements in tissues, and the relationships between the main leaf economicstraits. The variation in traits and differences among phylogeographic groups are theninterpreted with respect to patterns of Phragmites global distribution, with a focus ontheir invasiveness. We also explored bivariate relationships between some of the traitsmeasured and tested for the isometric or allometric growth of individual populations.

Materials and methods

Study species

The taxonomy of the genus Phragmites has developed rapidly over the past decade, andfive species are currently accepted: P. australis, P. frutescens, P. japonicus, P. mauritianus

and P. karka (Lambertini et al. 2006, Meyerson et al. 2012). Phragmites australis (Cav.)Trin. ex Steud. (Poaceae) is tall, helophytic, wind-pollinated perennial grass with shootsup to 4 m tall (but see Rodewald-Rudescu 1974 who report up to 6 m), forming an exten-sive system of rhizomes and stolons (runners), with a single inflorescence developing oneach fertile shoot, producing 500–2000 seeds (see Packer et al. 2017 and referencestherein). Phragmites australis represents one of the most ploidy-variable species known,with published cytotypes from 4x to 12x, based on x = 12 (te Beest et al. 2012), and thereis marked phylogeographic genetic diversity within the species and the whole genus(Saltonstall 2002, Lambertini et al. 2006).

This is relevant from the perspective of the global P. australis invasion: there area number of phylogeographic groups delimited based on an increasing knowledge of theworldwide distribution of haplotypes (Saltonstall 2002, Lambertini et al. 2006, 2012b,Meyerson & Cronin 2013, Lambertini 2016). The knowledge on the worldwide distribu-tion and status of populations is still incomplete; insights into the presence of non-nativegenotypes in the well-researched area of North America (Saltonstall 2002, Lambertini etal. 2012a, b) suggest that the distribution of alien genotypes is a much more widespreadphenomenon. In North America, there is evidence of multiple introductions of P. austra-

lis to this continent (Lambertini et al. 2012a, b, Meyerson et al. 2012, Meyerson & Cronin2013), with the European haplotype M being the first lineage recorded, as evidenced byan herbarium record �150 years ago (Saltonstall 2002). Alien lineages of P. australis,including haplotypes M and Delta, are expanding in North America and sometimes formmonospecific stands.

The recent account on the global distribution of P. australis revealed that this speciesis on all continents except Antarctica, and although in many regions of the world the ori-gin status is unclear and requires further study, there is evidence of weedy populationsbeing present in North America, Australia, and Madagascar (Packer et al. 2017). The spe-cies is now naturalized on islands in the Pacific (New Caledonia, Cook Islands and

Pyšek et al.: Invasion of Phragmites australis 53

Hawaii) and the Caribbean Sea (Bahamas, Dominican Republic, Haiti, Leeward Islands,Puerto Rico, Trinidad-Tobago and Windward Islands; see Fig. 2 in Packer et al. 2017).Whether alien genotypes of P. australis have been introduced to other places such asSouth America requires further study (Packer et al. 2017).

Ecology of Phragmites invasion

In its invaded range in North America, P. australis subsp. australis has converted botani-cally diverse wetlands into low-diversity ecosystems and outcompetes the North Ameri-can native P. australis subsp. americanus (Meyerson et al. 2000). The invasion is facili-tated by disturbance (Chambers et al. 1999, Meyerson et al. 2000, Silliman et al. 2014),but invasive populations also readily colonize undisturbed ecosystems. Invading popula-tions can be locally limited by poor drainage, lack of burial opportunities for seed and rhi-zome fragments, or by salinity during the early stages. However, naturalized alien popu-lations are reported to extend into less favourable anoxic and highly saline areas (Bart &Hartman 2002). Among reported predictors of invasiveness, such as vigorous growth,sexual reproduction, long-distance dispersal and genetic diversity (Belzile et al. 2010,McCormick et al. 2010, Kettenring et al. 2011, Kirk et al. 2011), an important role isplayed by genome size as a trait relating to competitiveness (Pyšek et al. 2018). Smaller-genome plants of the alien haplotype M outcompete native haplotypes with largergenomes in North America (Suda et al. 2015, Meyerson et al. 2016a, Pyšek et al. 2018).

Phylogeographic groups used in the experiment

Plants were grown in the Experimental Garden of the Institute of Botany of The CzechAcademy of Sciences in Průhonice, Czech Republic (49°59'39''N, 14°33'58''E), 320 ma.s.l., with a mean annual temperature of 8.6 °C and precipitation of 610 mm. We distin-guished six phylogeographic groups (see Fig. 1 for their global distribution). We usedP. australis clones obtained from the collections of the University of Rhode Island,Kingston, Rhode Island, USA and University of Aarhus, Denmark, and also includedsome field-collected clones. The phylogeographic groups were represented by popula-tions from (i) Australia; (ii) Europe; North America, with two groups including (iii)native (coded as ‘NAmerica-nat’) and (iv) invasive populations introduced from Europe(‘NAmerica-inv’); (v) South Africa (‘SAfrica’); and (vi) Far East. There were 17, 21, 17,19, 8, and 7 genotypes planted for each group, respectively, grown in a total of 372 pots.We used P. australis genotypes representing distinct populations (see Electronic Appen-dix 1 on the localities from which the clones used in the study were sampled).

Data collation: experimental set up

The clones were grown in round pots 60 cm in diameter at the top, 36 cm in height (effec-tive pot size 80 l), filled with sand and mixed with 480 g of slow-release (release time12–14 months) fertilizer Osmocote Pro (16% N, 11% P, 10% K). A piece of young rhi-zome (standard size of 20–30 cm) with an emerging shoot was planted in each pot on 7–8July 2012. Two to six replicates per clone, depending on the availability of the plant mate-rial and early survival were used, giving a total of 273 pots with experimental plants. Theplants were watered daily in the morning and in the evening using tap water delivered by

54 Preslia 91: 51–75, 2019

an automatic watering system (Hunter Industries, San Marcos, USA). To ensure compa-rable water supply to all plants, three holes were drilled in each pot 25 cm from the bot-tom to allow drainage of excessive water and achieve the same water level in each pot. InSeptember when some plants started to exhibit signs of iron-deficiency (yellowing), 0.2 gFe as iron in chelation complex of DTPA dissolved in 300 ml of tap water was added to allpots. Plants grew until full senescence (November), and the pots were covered over win-ter to protect the plants from frost. In early April of the following year, the frost protec-tion was removed, and 200 g of slow-diluting Osmocote and 0.2 g Fe were added to eachpot, and an addition of the same Fe dose was repeated in May/June. The experiment wasterminated after 2.5 yrs, in autumn 2014. For harvest, the aboveground biomass was cutabout 3 cm above the sand surface, when shoots were senescent (turning tan coloured) inlate November/early December of 2012 and 2013. During the final harvest in October2014, belowground biomass was also harvested, excavated from the substrate, rinsed andseparated into roots and rhizomes, and the length of each rhizome was measured. Theroot and rhizome biomass was oven-dried at 60 °C and weighed in the same way as foraboveground biomass (see Pyšek et al. 2018 for more details).

Traits measured

During the experiment we recorded information about a wide range of traits functionallyrelated to growth, physiology, tissue chemistry, reproduction, and herbivory (for a com-plete list of all traits recorded and details on methods of recording, see Table 1). Here wefocus on exploring the differences among the above phylogeographic groups in their per-formance with respect to the following traits: shoot height; shoot basal diameter; shootnumber per pot; aboveground dry biomass; belowground dry biomass separated into


Fig. 1. Global distribution of the six phylogeographic groups with sampling location of populations used in thepresent study.

56 Preslia 91: 51–75, 2019

Tab

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Roo

tN(%

)R

ootN

conc

entr

atio

n(f

orde

tail

sse

ero

otC

and

leaf

C)

9–10

/201

4

Roo

tP(m

g·kg

–1)

Roo

tPco

ncen

trat

ion

(for

deta

ils

see

root

Can

dle

afP

)9–

10/2

014

roots and rhizomes; total length of rhizomes in the pot (growth traits); proportional allo-cation of biomass to generative reproduction (panicle weight, a reproductive trait); leafwater content; specific leaf area (SLA); leaf area per shoot; leaf toughness measured asthe force necessary to penetrate the leaf; photosynthetic capacity measured on fullydeveloped top leaf (physiological traits); C, N, P concentration determined separately inleaves, roots and rhizomes, and used to calculate ratios (tissue chemistry). The overviewof the traits measured with details on how and when they were sampled is in Table 1. Forthe majority of growth traits, we used data from the 2013 growing season to avoid theeffect of possible space limitation (including the aboveground biomass), with the excep-tion of traits related to belowground harvest in 2014 (including the belowground / above-ground biomass).

Statistical analysis

All analyses were carried out in R (v. 3.4.0, R Core Team 2017). First, we used linearmixed-effect models to test the performance of individual traits, with phylogeographicgroups as the fixed factor and genotype identity as a random factor. Second, the same datawas averaged per genotype and the averaged values were used in a one-way analysis ofvariance (ANOVA) to test for the significance of differences among the phylogeographicgroups. As the results from these two analyses were identical, only the one-way ANOVAresults based on the clone mean data are shown. Bonferroni post-hoc correction was usedfor traits that showed significant differences in ANOVA. The normality and homogeneityof the trait variances were checked, and log-transformation was applied when needed.For variables not meeting the assumptions of ANOVA, non-parametric Kruskal-Wallisrank sum test was used, followed by a Dunn post-hoc test if a significant difference wasdetected.

As shoot number and shoot height were measured more than once during 2013 and2014, linear mixed models were applied to these two traits, with years and phylogeo-graphic groups as main factors, and the measurement times and genotype identities asrandom factors. Linear mixed models were applied via “lmer” function from the lmerTestpackage (Kuznetsova et al. 2017). We ran pairwise post-hoc comparisons using least-squared (LS) means with Bonferonni corrections applied to ensure the global Type I errorrate remained at 0.05 via the ‘emmeans’ package (Lenth et al. 2018). All previous modelswere examined by diagnostic plots to check if they met the assumptions of linearregression.

To investigate the bivariate relationships between traits, in particular those related tothe leaf economics spectrum (LES) and biomass allocation, the standardized major axis(SMA) analysis (Wright et al. 2004) was implemented with the smatr package in R(Warton et al. 2012) using clone means. SMA line fitting minimizes residual variance inboth x and y dimensions and is preferred in analysing bivariate allometric relationships(Warton et al. 2006). We specifically focused on the leaf economics traits, i.e. leaf N, leafP, leaf mass per area (LMA), and Amax, to test whether bivariate trait relationships ofP. australis populations are similar to the corresponding ones from the Global Plant TraitNetwork (GLOPNET) dataset (Wright et al. 2004). The GLOPNET dataset reports val-ues of photosynthetic capacity (Amax), dark respiration rate, nitrogen (N) and phosphorus(P) concentrations, leaf life span (LL), and LMA, and covers 2222 species from 175 sites

58 Preslia 91: 51–75, 2019

on six continents. We ran a similar analysis on the biomass allocation to different organparts to test for the isometric or allometric growth of the P. australis populations(Komiyama et al. 2008).

Principal components analysis (PCA) with all traits measured in this study wasapplied to examine the pattern of the six phylogeographic groups, and how close they areto each other. PCA was run via the FactoMineR package (Lę et al. 2008).

Results

European native populations and those originating from Europe that are invasive in NorthAmerica were the most productive, with the former producing the greatest belowgroundand the latter aboveground biomass. These values were markedly greater than thoserecorded for populations from other phylogeographic groups (with the exception of FarEastern populations that exhibited comparable values), and those populations also pro-duced a great root biomass. Consequently, European populations had the greatest below-ground / aboveground biomass ratio and root / aboveground biomass ratio, which were,however, not significantly different from that obtained for Far Eastern populations. Thethree groups mentioned above also invested a great proportion of biomass into generativereproduction. North American native populations were less productive than both Euro-pean-related groups and were similar in this respect to South African and Australian pop-ulations. South African populations produced rather thick shoots with a large leaf areaand tough leaves. Far Eastern populations had the longest rhizomes, while North Ameri-can native, African and Australian populations the shortest. The Far Eastern populationshad also the greatest SLA (see Table 2 for values and significances of these differences).No significant differences among phylogeographic groups were found in photosynthesis.

These results indicate that there are differences among populations that were alsomanifested in shoot number per pot and partly height (Fig. 2). European native and FarEastern populations produced more shoots than other groups except North Americaninvasive that produced comparable numbers of shoots. Of the three most vigorousphylogeographic groups, European native produced more shoots per pot than NorthAmerican invasives, although this difference was less pronounced (Fig. 2). The differ-ences in shoot height among phylogeographic groups were generally non-significantwith the only exception being that Australian populations performed poorly in compari-son with European and both groups of North American plants (Fig. 2).

There were few significant differences in C, N, P concentrations in leaves, rhizomesand roots (Table 3). European native and the Far Eastern populations were often amongthose with the highest concentrations and North American natives often had the lowestconcentrations of these elements.

The trait values we recorded for the P. australis populations were distributed withinthe range of the GLOPNET dataset (Fig. 3). Compared to this global species dataset,P. australis, pooled across phylogeographic groups, tends to have higher Amax, N and Pconcentrations, and lower LMA. Bivariate trait relationships were generally consistentwith the results from the GLOPNET dataset (Wright et al. 2004), with the exception ofLMA–N and N–P relationships the slopes of which were significantly different fromglobal species data.


60 Preslia 91: 51–75, 2019

Tab

le2.

–M

ean

valu

es(±

1S

D)

ofbi

omas

s,gr

owth

and

phys

iolo

gica

ltra

its

ofP

hra

gm

ites

au

stra

lis

byph

ylog

eogr

aphi

cgr

oups

.F-v

alue

san

dP

-val

ues

ofA

NO

VA

test

sar

egi

ven;

diff

eren

tsup

ersc

ript

sro

w-w

ise

indi

cate

sign

ific

antd

iffe

renc

esbe

twee

nth

ere

spec

tive

phyl

ogeo

grap

hic

grou

ps(P

<0.

05).

Not

eth

atn

for

leaf

toug

hnes

sis

20,a

nd7

forE

urop

ean

dS

outh

Afr

ica,

resp

ecti

vely

.SL

A,s

peci

fic

leaf

area

;Am

ax,p

hoto

synt

heti

cca

paci

ty.R

epro

duct

ive

allo

cati

onis

nots

how

nfo

rAus

tral

ian

and

Sou

thA

fric

anpo

p-ul

atio

nsdu

eto

poor

gene

rati

vere

prod

ucti

onat

the

end

ofth

eex

peri

men

t.T

hebo

ldva

lues

indi

cate

the

grou

pw

ith

the

high

estv

alue

sin

the

resp

ecti

vetr

ait,

rega

rdle

ssof

the

sign

ific

ance

ofth

edi

ffer

ence

.

Tra

its

Aus

tral

ia(n

=17

)E

urop

e(n

=21

)F

arE

ast

(n=

7)N

Am

eric

a-in

v(n

=17

)N

Am

eric

a-na

t(n

=19

)S

Afr

ica

(n=

8)F

-val

ueP

-val

ue

Rhi

zom

ebi

omas

s(g

)41

1.3±

274.

1a12

96.5

±39

0.4c

1063

.0±

229.

8bc92

3.5±

190.

7b53

8.3±

301.

1a45

2.0±

212.

8a25

.15

<0.

001

Roo

tbio

mas

s(g

)16

2.6±

128.

2a49

6.5±

149.

5c50

9.2±

171.

0c37

8.6±

133.

3bc22

7.5±

134.

9a20

3.2±

120.

0ab17

.16

<0.

001

Bel

owgr

ound

biom

ass

(g)

573.

9±39

0.0a

1792

.9±

488.

7c15

72.2

±33

4.2bc

1302

.1±

262.

6b76

5.8±

428.

3a65

5.2±

316.

0a26

.44

<0.

001

Abo

vegr

ound

biom

ass

(g)

271.

3±21

9.7a

1231

.3±

353.

4cd84

2.52

±12

6.5bc

1304

.0±

199.

8d62

4.8±

446.

5b61

6.2±

282.

6ab27

.80

<0.

001

Bel

ow:a

bove

grou

ndbi

omas

s0.

62±

0.29

a2.

19±

1.00

d1.

88±

0.55

cd1.

25±

0.30

bc0.

92±

0.35

ab0.

69±

0.16

ab20

.09

<0.

001

Roo

t:ab

oveg

roun

dbi

omas

s0.

18±

0.08

a0.

57±

0.28

d0.

55±

0.25

cd0.

35±

0.13

bc0.

26±

0.09

b0.

21±

0.09

ab18

.41

<0.

001

Rhi

zom

ele

ngth

(cm

)40

03.5

±26

28.3

a15

199.

8±43

62.7

b22

607.

8±39

34.2

c14

653.

0±39

63.0

b57

08.5

±33

56.8

a38

80.1

±20

98.2

a51

.05

<0.

001

Ste

mdi

amet

er(m

m)

4.87

±1.

05b

4.62

±0.

86b

3.53

±0.

33a

4.64

±0.

49b

5.68

±0.

61c

6.85

±1.

02d

18.3

8<

0.00

1

Am

ax(μ

mol

CO

2m

–2·s

–1)

20.3

±5.

321

.7±

2.7

19.0

±2.

720

.9±

1.9

18.5

±3.

221

.7±

2.9

2.40

0.04

4

SL

A(m

2 ·kg–1

)12

.7±

1.6a

13.0

±1.

2a15

.0±

1.4c

13.3

±0.

8ab13

.4±

1.8ab

12.2

±1.

1a3.

750.

004

Lea

far

ea(m

m2 )

2849

.6±

1413

.5a

3755

.5±

1259

.2ab

c30

25.0

±55

9.2ab

4279

.9±

620.

4bc45

85.4

±11

57.1

c44

34.3

±73

7.1bc

6.35

<0.

001

Lea

far

eape

rsh

oot(

cm2 )

231.

5±10

5.5ab

311.

9±14

8.5bc

147.

2±23

.3a

354.

6±93

.5c

330.

5±12

0.0bc

374.

1±93

.3c

5.50

<0.

001

Lea

fw

ater

cont

ent(

%)

65.7

±1.

7c60

.6±

2.5a

62.0

±1.

6ab59

.3±

1.5a

63.1

±3.

7b67

.0±

1.4c

20.2

0<

0.00

1

Rep

rodu

ctiv

eal

loca

tion

(%)

–4.

42±

3.95

ab5.

41±

2.78

ab7.

60±

4.28

b1.

97±

4.06

a–

6.12

0.00

1

Lea

fto

ughn

ess

(N)

4.18

±1.

36a

3.98

±1.

21a

3.06

±0.

84a

3.81

±0.

56a

4.36

±1.

10a

6.24

±1.

17b

73.5

20.

006


Tab

le3.

–M

ean

valu

es(±

1S

D)

ofC

,N,P

and

thei

rra

tios

inle

af,r

oot,

and

rhiz

ome

tiss

ues

ofP

hra

gm

ites

au

stra

lis

byph

ylog

eogr

aphi

cgr

oups

.F-v

alue

san

dP

-val

ues

ofA

NO

VA

test

sar

egi

ven;

diff

eren

tsup

ersc

ript

sro

w-w

ise

indi

cate

sign

ific

antd

iffe

renc

esbe

twee

nth

ere

spec

tive

phyl

ogeo

grap

hic

grou

ps(P

<0.

05).

The

bold

valu

esin

dica

teth

egr

oup

wit

hth

ehi

ghes

tval

ues

inth

ere

spec

tive

trai

t,re

gard

less

ofth

esi

gnif

ican

ceof

the

diff

eren

ce.

Tra

itA

ustr

alia

(n=

17)

Eur

ope

(n=

21)

Far

Eas

t(n

=7)

NA

mer

ica-

inv

(n=

17)

NA

mer

ica-

nat

(n=

19)

SA

fric

a(n

=8)

F-v

alue

P-v

alue

Lea

fC

(mg·

g–1)

438.

5±6.

944

0.1±

4.5

438.

2±4.

843

7.6±

2.9

442.

0±5.

443

7.2±

4.6

2.05

0.08

0

Lea

fN

(mg·

g–1)

34.9

±3.

6bcd

37.9

±3.

0d38

.8±

5.6d

34.4

±2.

9abc

31.0

±4.

3a31

.2±

1.6ab

10.7

9<

0.00

1

Lea

fP

(mg·

g–1)

2.11

±0.

36ab

c2.

11±

0.20

bc2.

27±

0.46

c1.

86±

0.22

ab1.

82±

0.33

a2.

00±

0.27

abc

4.36

0.00

1

Lea

fC

:N12

.8±

1.5ab

11.7

±0.

9a11

.6±

1.6a

13.0

±1.

1ab14

.8±

2.3c

14.2

±0.

9bc10

.33

<0.

001

Lea

fN

:P17

.0±

2.63

ab18

.2±

0.8bc

17.4

±2.

3abc

18.8

±1.

2c17

.5±

1.2ab

c15

.9±

1.5a

4.13

0.00

2

Roo

tC(m

g·g–1

)41

2.8±

19.6

a43

8.7±

9.3b

426.

0±13

.1ab

439.

7±15

.5b

432.

2±13

.4b

430.

6±10

.9ab

8.22

<0.

001

Roo

tN(m

g·g–1

)14

.2±

4.9

14.1

±2.

814

.7±

1.0

12.0

±1.

912

.3±

1.6

13.3

±3.

42.

010.

086

Roo

tP(m

g·g–1

)1.

41±

0.53

c1.

02±

0.19

ab1.

28±

0.10

bc0.

84±

0.16

a1.

17±

0.27

bc1.

22±

0.19

bc7.

45<

0.00

1

Roo

tC:N

32.8

±9.

033

.4±

7.0

29.8

±2.

1839

.0±

7.1

37.1

±4.

836

.9±

9.8

2.46

0.04

0

Roo

tN:P

11.2

±3.

7a14

.1±

2.1ab

12.0

±1.

19ab

15.1

±2.

6b11

.4±

2.3a

11.1

±2.

1a7.

12<

0.00

1

Rhi

zom

eC

(mg·

g–1)

430.

6±10

.7b

430.

1±5.

4b43

5.0±

5.5b

423.

8±9.

8ab41

8.1±

18.5

a41

7.8±

8.8ab

4.74

<0.

001

Rhi

zom

eN

(mg·

g–1)

18.0

±3.

8a23

.0±

3.4c

23.0

±3.

6bc19

.0±

2.4ab

17.5

±3.

0a19

.5±

3.1ab

c8.

65<

0.00

1

Rhi

zom

eP

(mg·

g–1)

2.05

±0.

39ab

2.29

±0.

38b

2.19

±0.

332.

04±

0.30

ab1.

87±

0.30

a2.

01±

0.34

ab3.

360.

008

Rhi

zom

eC

:N26

.9±

6.6b

19.7

±3.

4a19

.7±

3.1a

24.1

±4.

2ab26

.5±

3.9b

22.7

±4.

1ab6.

69<

0.00

1

Rhi

zom

eN

:P9.

19±

2.19

10.2

1±1.

6810

.58±

0.88

9.59

±1.

309.

58±

1.32

10.0

6±1.

312.

480.

038

There were significant differences in biomass allocation to different organs and acrossall the studied P. australis populations with plants showing an allometric growth (Fig. 4).The plants allocated more biomass to belowground than aboveground organs.

The PCA of phenotypic traits for the six phylogeographic groups revealed that Euro-pean native, Far Eastern and North American invasive populations were least distinctfrom each other, forming a group that almost does not overlap with the other three. NorthAmerican native populations cannot be separated from South African and Australianpopulations based on their traits (Fig. 5A). The factor loadings of the PCA generally fit-ted the previous analyses, i.e., the former three groups tend to have more shoots, longerrhizome, higher belowground biomass, and higher leaf N than the latter three groups,which showed larger stem diameter (Fig. 5B)

62 Preslia 91: 51–75, 2019

Fig. 2. – Least squared (LS) means and SEs of the (A) shoot number and (B) shoot height of the sixphylogeographic groups of Phragmites australis, based on the linear mixed models. As there was no signifi-cant difference between years, the values were pooled together. Different letters above the error bars indicatesignificant differences among groups (P < 0.05), tested via Bonferroni post-hoc correction.


Fig. 3. – Slope tests in standardized major axis (SMA) lines for the bivariate allometric relationship betweenleaf economics spectrum (LES) traits for P. australis populations and the GLOPNET datasets (Wright et al.2004). The circles in background are data from GLOPNET (Wright et al. 2004). Dashed lines represent non-significant relationship between the traits (P > 0.05) and solid lines are significant (P < 0.05); if the relationshipbetween traits is non-significant (P > 0.5), no SMA test was run.* indicates significant difference between thetwo slopes: ** P < 0.01, *** P < 0.001. LMA: Leaf mass per area, the inverse of SLA; Nmass and Pmass, phospho-rus and nitrogen concentration on mass bases, respectively; Amax, photosynthetic capacity.

64 Preslia 91: 51–75, 2019

Fig. 4. – Allometric relationships between biomass of different organ parts. Dashed lines represent isometricline (slope = 1), solid red lines represent significant relationships between variables; significant differencesbetween the two slopes are indicated: * P < 0.05.

Fig. 5. – (A) Principal components analysis (PCA) using all measured phenotypic traits for the sixphylogeographic Phragmites australis groups. The square and circle with the same color as surrounding pointsis the centroid and 95% confidence ellipse of the specific phylogeographic group. (B) Factor loadings of thePCA. The black arrows with names are the traits with coefficients of higher than 0.6, whist the gray arrows aretraits with low coefficients (lower than 0.6). �

Discussion

Differences among phylogeographic groups

In the previous paper based on the same dataset, we found a distinct relationship betweengenome size and invasiveness at the intraspecific level; monoploid genome size was theonly significant variable that clearly separated the North American native plants frominvading populations of European origin. The latter had a smaller genome that was asso-ciated with plant traits favoring invasiveness such as long rhizomes, early emergingabundant shoots, low aphid attack and low C / N ratio (Pyšek et al. 2018). In this study themain focus is on characterizing a broader range of phylogeographic groups by their phys-iological traits.

In general, both phylogeographic groups with origins in Europe – be it those that growas native in this continent or as invaders in North America – are more vigorous than allother groups, with the exception of the Far Eastern populations that reached the highestvalues in some characteristics. They produced high biomass, tall shoots and dense stands.The native European populations had the greatest belowground / aboveground biomassratios, while the North American invasives allocated a greater proportion of biomass intogenerative reproduction, measured as the relative weight of the panicle. On the otherhand, North American native populations performed rather poorly in terms of biomassproduction and were similar in this respect to South African populations. Australianplants were on average even shorter and less vigorous. However, their poor performancecould also be at least partly due to fact that the environmental conditions in which theplants were grown might have been suboptimal for these plants – the performance of thisgroup need therefore to be interpreted with caution.

Overall, these results correspond with the invasion success of European plants inNorth America and suppression of the native North American populations in direct com-petition with the invader (Meyerson et al. 2000). Based on the performance of various lin-eages in our experiment, invasion by Australian and African populations in the NorthernHemisphere due to weak environmental match or genetic differences seems unlikely atpresent. However, it is not possible to exclude the invasion of genotypes of European ori-gin into Southern Hemisphere or other temperate regions. Unfortunately, reciprocaltransplant experiments that could either support or contradict this hypothesis are missing.

A novel result of the present study is the vigour of the Far Eastern populations, whichis comparable to that of the European and North American invasive populations. Besidesthe high biomass of the Far Eastern populations, their invasion potential may be enhancedby extensive lateral spread by long rhizomes. Achenbach et al. (2012) demonstrated thatthe Far Eastern populations grew even taller and performed better than the Europeangenotypes in a common garden study in Denmark. However, the superior performance ofthe Far Eastern genotypes over the Australian populations (their close relatives) in sev-eral traits was not expected. In Lambertini et al. (2006) the Far Eastern populationsappeared as a monophyletic group within the Australian clade of P. australis, with whichit shares also the chloroplast DNA (haplotype P) (Lambertini et al. 2012b). Sucha phenotypic divergence in traits, related to competitiveness and fitness between the twoclosely related groups, would be a new wrinkle in Phragmites evolutionary history. Pos-sible explanations could be that the Far Eastern populations acquired the competitivetraits and became similar to the European populations by hybridization. Far East Asia is

66 Preslia 91: 51–75, 2019

a hot spot of Phragmites lineages, including European haplotypes (An et al. 2011), andrecombination between lineages may have occurred. However, for our experimental con-ditions the more probable explanation seems to be the better environmental match for theFar Eastern populations as well as for those of the Northern Hemisphere. The poor per-formance of the North American native populations does not contradict this explanationas these populations are generally less competitive than European populations (Pyšek etal. 2018). Nevertheless, these new insights of the present study require further testing,ideally by reciprocal transplants of Eurasian and Australian plants, and should stimulatefurther genetic research both in the Far East and North American native populations.

A pattern seems to emerge if the position of the Phragmites populations in the ordina-tion space, and their geographical distribution, is interpreted with respect to the latitude(reflecting solar radiation) and climatic conditions of the sites of origin. The PCA analy-sis shown in Fig. 5 indicates that the phylogeographic groups are divided into two distinctclusters, one being Australia, South Africa and North American native clones, the otherthe Far-East clones, European ones and North American invasives. With the exception ofNorth American populations, where native and invasive grow together, populations fromthe former group tend to originate from relatively low-latitude and warmer regions, whilethe latter from higher-latitude colder regions (Electronic Appendix 1). The warmer con-ditions and high solar radiation appear to be associated with lower shoot densities and, inthe case of Australian populations, with relatively low aboveground biomass, comparedto belowground. One explanation of the weaker performance of these populations in ourexperiment could be that populations adjusted to warm conditions and high solar radia-tion, such as Australian or South African, need to allocate more biomass to rhizome sys-tem for the survival during winter if they are growing under cold climate and low solarradiation of the Czech Republic. This would be supported by previous research on thevariation in growth response of Phragmites with changing geographical conditions(Granéli et al. 1992, Clevering et al. 2001, Karunaratne et al. 2003, Cronin et al. 2015,Allen et al. 2016, Bhattarai et al. 2016).

Biomass production

Phragmites australis is among the most thoroughly researched plant species (Meyersonet al. 2016b) and a great body of information on growth and biomass production undera wide range of conditions has accumulated over last decades, including belowgroundproduction (e.g. Dykyjová & Hradecká 1976, Fiala 1976, Granéli et al. 1992, Čížková etal. 2001, Šantrůčková et al. 2001). Although none of the studies systematically comparedthese characteristics for such a high number of lineages under standardized conditions ofan experimental garden, it is of interest to review this information here and compare withour data.

Except belowground production recorded in Australia (see Packer et al. 2017 and cita-tions therein) and in a hypertrophic lake in the United States (Boyd et al. 2015), theabove- and belowground biomass recorded in our experiment was generally high andespecially values for European clones exceeded field values reported from Europe(Čížková et al. 1996, Kuhl et al. 1997, Soetaert et al. 2004, Gribsholt et al. 2007); thesame was true for belowground / aboveground biomass ratio (Coops et al. 1996, Soetaertet al. 2004). The North American clones in our experiment, namely the invasive, also pro-


duced more above- and belowground biomass (Minchinton & Bertness 2003, Emery &Fulweiler 2014) and higher belowground / aboveground ratio than North American fieldpopulations (Farnsworth & Meyerson 2003, Achenbach & Brix 2014), and similar bio-mass to those reported from cultivation (Hellings & Gallagher 1992). The greater bio-mass in the experiments indicates that plants were not limited by the lack of resources.These results further support the high resource-use efficiency, when resources are avail-able, of the European populations and their resilience at the high levels of our fertiliza-tion, at least in this European common garden.

Nitrogen, phosphorus and carbon in leaves, rhizomes and roots

High nutrient content in the tissues of European native and Far Eastern populations agreewith their high invasive potential indicated by their vigorous growth, and also with the inva-sion success of European clones in North America (Meyerson et al. 2009). The leaf-nitro-gen values in our experiment were close to the maxima found in plants cultivated underhigh supply of nutrients (Clevering 1998) and to the maxima found in the field (Kohl et al.1998, Farnsworth & Meyerson 2003, Baldantoni et al. 2004, Soetaert et al. 2004, Elvisto2010). The pattern of the highest leaf-nitrogen values in European clones followed by NorthAmerican invasive and North American native genotypes (Guo et al. 2014) was confirmedin our experiment. Also the leaf-carbon values were close to maxima of 455–465 mg·g–1

reported from the field for European (Csatari et al. 2015) and North American invasiveplants (Schaefer et al. 2014). The leaf phosphorus was comparable with the values, includ-ing maxima of 2.5–2.9 mg·g–1, reported from the field in Europe (Baldantoni et al. 2004,Elvisto 2010, Flury & Gessner 2014, Marchand et al. 2014).

The rhizome nitrogen values were comparable with the highest values measured onplants in the field and in cultivation in Europe (Čížková & Lukavská 1999 and Clevering1998, respectively). Rhizome carbon in the experimental garden was within the range ofvalues known from Europe (Engloner et al. 2004, Csatari et al. 2015) and rhizome phos-phorus reached values comparable with the highest values found in the field in this conti-nent (Čížková & Lukavská 1999).

The root nitrogen values corresponded to the maxima of 24–26 mg·g–1 found in culti-vation in Europe (Clevering 1998) and root carbon was within the range of values mea-sured there (Hartmann 1999, Csatari et al. 2015). Unlike the other elements the values ofroot phosphorus rather compared to lower values found in Europe (Duan et al. 2004,Engloner et al. 2004, Stamati et al. 2010).

The high values of leaf and rhizome nitrogen and phosphorus, as well as of the rootnitrogen, indicate a very good nutrient supply to the cultivated plants which, togetherwith the generally high biomass values recorded in this experiment, indicate that theplants were not limited by space and nutrients. However, it needs to be kept in mind thatthe plants in our experiment were cultivated under optimal conditions and actual fieldperformance may be limited by low resource availability, disturbance or stress.

Leaf traits

The photosynthetic capacity (Amax) values in our experiment can be compared to the max-ima reported in the literature, for some European and North American invasive clones ofP. australis cultivated in a common garden (Hansen et al. 2007 and Mozdzer et al. 2016).

68 Preslia 91: 51–75, 2019

In a previous study, Guo et al. (2014) compared the photosynthesis of North Americaninvasive and native clones with native European plants and found the highest values inthe first of the three groups. We did not find significant differences between these lin-eages in our study, but the American native clones had considerably lower photosynthesisthan the other two groups of European origin. Plants in the previous study had rather lowleaf-nutrient content (Guo et al. 2014), which can limit the photosynthetic output andmight have thus generated the differences between the three groups.

In a previous study from China, leaf economics traits of P. australis showed largeintraspecific variation (Hu et al. 2015). The specific leaf area (SLA) values recorded in ourexperiment are within the upper half of the range reported for European, Asian and NorthAmerican plants (Farnsworth & Meyerson 2003, Soetaert et al. 2004, Colmer & Pedersen2008, Jiang et al. 2009, Shi et al. 2010, Eller et al. 2014, Li et al. 2014, Zhong et al. 2014).Such relatively high values are probably due to a high nutrient supply as increased nitrogenavailability was revealed to increase SLA (Minchinton & Bertness 2003).

Higher Amax, N and P concentrations, and higher SLA of P. australis compared toother GLOPNET plants is probably the reason for it growing so vigorously and beinggenerally successful throughout the temperate zone. In accordance with this, the mostproductive European and North American invasive clones are at the positions most dis-tant from the LMA–N and N–P relationships within the GLOPNET plants (Fig. 3).

Post-introduction changes in the Phragmites complex

Within our study system, the natural experiment created by the historical intercontinentalintroductions of P. australis provided an opportunity to address not only the ecologicaldifferences between native North American populations and invasive populations intro-duced from Europe, but also to explore post-introduction evolutionary change in the lat-ter (Pyšek et al. 2018). This can be achieved by comparing North American invasive pop-ulations originating from Europe with their ancestors that still occur as natives in Europe.In fact, the position of populations in the PCA seems to confirm this. European popula-tions, both the native sampled in Eurasia and those that were derived from Europeanancestors and that now invade in North America (Pyšek et al. 2018), have much in com-mon in terms of the trait space that they occupy in the ordination space; together theyform a distinct group not overlapping with populations from other continents. This corre-sponds to the results of Guo et al. (2014) and Bui et al. (2016) who similarly found thethree groups largely separated but used a different method. However, the North Americaninvasives in our experiment were closer to North American natives than they were to theiroriginal European ancestors, possibly reflecting the effect of the environment after atleast 200 years of invasion (Guo et al. 2018) or interbreeding.

Nevertheless, these inferences are weakened because we do not have exact informa-tion that would allow us to relate particular native European genotypes to the specificgenotypes introduced to North America. Therefore, the biogeographical comparisonamong European and North American populations is made by randomly sampling geno-types in the two ranges that represent the three groups defined by origin. Several studieshave attempted to identify the source European populations of the introduced populationsin North America, but so far none have succeeded, and at present it is very unlikely thatsource populations can be back-traced. This is because the populations within European


phylogeographic group are very diverse and each genotype has its relatives very far fromits population (Lambertini et al. 2008). All of the European common reed isa metapopulation and this genetic pattern is due to the fact that (i) P. australis seeds andpollen are dispersed over long distances by wind and birds, (ii) P. australis has been usedand moved by humans in Europe (thatching, constructed wetlands, etc.), (iii) both thenative Eurasian and introduced North-American populations have evolved since theirseparation, and (iv) the North American invasive population is the result of multipleintroductions (Lambertini et al. 2006, 2012a, Meyerson & Cronin 2013). Nevertheless,we are convinced that the comparison of the phylogeographic groups sampled randomlyprovides valid insights into the physiological differences among P. australis phylogeo-graphic groups.

Limitation of the common-garden study and the need for further research

The results were obtained in a standard garden experiment and thus they need to be inter-preted with caution resulting from controlled settings. It has been shown that the perfor-mance of P. australis is influenced by environmental conditions such as water regime,nutrient availability, salinity, temperature and CO2-levels (see e.g. Engloner 2009, Elleret al. 2017, Packer et al. 2017 and references herein). Also, interaction of the effects ofcultivation environment with individual populations on some growth characteristics havebeen reported (Clevering et al. 2001). This is especially relevant for Australian and SouthAfrican clones for which the growing conditions in central Europe differ most from theoriginal sites, including the summer/winter switch that may influence biorhythms, poten-tially manifested in the absence of flowering. However, it was logistically impossible tomanipulate growing conditions in such an extensive experiment, where the aim of cover-ing most of the world distribution ranges of P. australis was given priority.

See www.preslia.cz for Electronic Appendix 1

Acknowledgements

The study was supported by projects no. 14-15414S, and no. 14-36079G Centre of Excellence PLADIAS(Czech Science Foundation), and long-term research development project RVO 67985939 (The Czech Acad-emy of Sciences). P. Pyšek acknowledges support by Praemium Academiae award from The Czech Academyof Sciences. We thank Michal Pyšek for logistic support, and Marie Brůnová, David Cmíral, DominikaPrajzlerová, Ivana Rajznoverová and Zuzana Sixtová for technical assistance. Funding was provided toL. A. Meyerson by the National Science Foundation DEB Award 1049914, the Fulbright Commission of theUnited States and the Czech Republic, and the University of Rhode Island College of Environment and LifeSciences Agricultural Experiment Station Project RI00H-332, 311000-6044.

Souhrn

Diferenciace v rámci jednoho ze světově nejrozšířenějších a nejvýznamnějších planě rostoucích kosmopolit-ních druhů, Phragmites australis, i invaze jeho jednotlivých linií mimo jejich domácí areály přitahuje stále vět-ší pozornost. Na základě experimentálního srovnání růstových a fyziologických vlastností 89 populací předsta-vujících odlišné genotypy ze šesti fylogeografických linií rákosu, pocházejících z Austrálie, Evropy, SeverníAmeriky (dvě skupiny zahrnující domácí populace a invazní populace zavlečené z Evropy), Jižní Afriky a Dál-ného Východu jsme zjistili diferenciaci populací do dvou velkých skupin. První zahrnuje populace z Evropy,invazní populace ze Severní Ameriky a populace z Dálného Východu, zatímco do druhé skupiny spadají popu-

70 Preslia 91: 51–75, 2019

lace z Austrálie a Jižní Afriky spolu s původními severoamerickými. Pro první skupinu je typický vitální růst,který se projevuje vyšší hustotou stébel v pěstební nádobě, největší podzemní biomasou evropských populací,nejdelšími oddenky a největší specifickou listovou plochou u populací z Dálného Východu, vysokou koncent-rací dusíku a fosforu v listech a oddencích a vysokým poměrem N:P v listech a kořenech populací z Evropya Dálného Východu. Severoamerické populace měly největší nadzemní biomasu a největší podíl biomasy in-vestované do generativní reprodukce. Hodnoty maximální fotosyntézy, koncentrací N a P v pletivech a speci-fické listové plochy naměřené napříč sledovanými populacemi P. australis se pohybují poblíž horní hranicerozsahu hodnot druhů zahrnutých do databáze GLOPNET. Zjištěné výsledky ukazují na nepravděpodobnostinvaze populací z Austrálie a Jižní Afriky na severní polokouli bez ohledu na to, zda kvůli genetické odlišnostipopulací nebo jejich špatnému přizpůsobení místním podmínkám. Na druhou stranu nelze vyloučit invazievropských populací do dalších oblastí, zejména na jižní polokouli.

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Received 16 July 2018Revision received 6 December 2018

Accepted 10 December 2018


physiology of a plant invasion: biomass production, growth ... et al-physiology of a plant...

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